scholarly journals Natural variation in the Arabidopsis AGO2 gene is associated with susceptibility to potato virus X

2019 ◽  
Author(s):  
Chantal Brosseau ◽  
Ayooluwa Adurogbangba ◽  
Charles Roussin-Léveillée ◽  
Zhenxing Zhao ◽  
Sébastien Biga ◽  
...  

AbstractRNA silencing functions as an anti-viral defence in plants through the action of DICER-like (DCL) and ARGONAUTE (AGO) proteins. However, there are few known examples of functional variation in RNA silencing components. The AGO2 protein is important for antiviral defense against multiple viruses and has been shown to be a major limiting factor to infection by potato virus X (PVX) of Arabidopsis thaliana but not Nicotiana benthamiana. We show that the AGO2 proteins from these two plants have differential activity against PVX, suggesting that variation in AGO2 is important in plant-virus interactions. Consistent with this, we find that the Arabidopsis thaliana AGO2 gene shows a high incidence of polymorphisms between accessions, with evidence of selective pressure. AGO2 protein variants can be assigned to two groups, in near equal frequency, based on an amino acid change and small deletions in the protein N-terminus. Inoculation of a large number of Arabidopsis accessions shows strong correlation between these alleles and resistance or susceptibility to PVX. These observations were validated using genetic and transgenic complementation analysis, which showed that one type of AGO2 variant is specifically affected in its antiviral activity, without interfering with other AGO2-associated functions such as anti-bacterial resistance or DNA methylation. Our results demonstrate a novel type of genetically-encoded virus resistance and suggest that plant-virus interactions have influenced natural variation in RNA silencing components.

2018 ◽  
Vol 20 (1) ◽  
pp. 469-477 ◽  
Author(s):  
Duc H. T. Le ◽  
Eduardo Méndez-López ◽  
Chao Wang ◽  
Ulrich Commandeur ◽  
Miguel A. Aranda ◽  
...  

2008 ◽  
Vol 21 (2) ◽  
pp. 178-187 ◽  
Author(s):  
Shahid Aslam Siddiqui ◽  
Cecilia Sarmiento ◽  
Erkki Truve ◽  
Harry Lehto ◽  
Kirsi Lehto

RNA silencing suppressor genes derived from six virus genera were transformed into Nicotiana benthamiana and N. tabacum plants. These suppressors were P1 of Rice yellow mottle virus (RYMV), P1 of Cocksfoot mottle virus, P19 of Tomato bushy stunt virus, P25 of Potato virus X, HcPro of Potato virus Y (strain N), 2b of Cucumber mosaic virus (strain Kin), and AC2 of African cassava mosaic virus (ACMV). HcPro caused the most severe phenotypes in both Nicotiana spp. AC2 also produced severe effects in N. tabacum but a much milder phenotype in N. benthamiana, although both HcPro and AC2 affected the leaf tissues of the two Nicotiana spp. in similar ways, causing hyperplasia and hypoplasia, respectively. P1-RYMV caused high lethality in the N. benthamiana plants but only mild effects in the N. tabacum plants. Phenotypic alterations produced by the other transgenes were minor in both species. Interestingly, the suppressors had very different effects on crucifer-infecting Tobamovirus (crTMV) infections. AC2 enhanced both spread and brightness of the crTMV-green fluorescent protein (GFP) lesions, whereas 2b and both P1 suppressors enhanced spread but not brightness of these lesions. P19 promoted spread of the infection into new foci within the infiltrated leaf, whereas HcPro and P25 suppressed the spread of crTMV-GFP lesions.


2006 ◽  
Vol 19 (8) ◽  
pp. 904-913 ◽  
Author(s):  
D. Barajas ◽  
F. Tenllado ◽  
J. R. Díaz-Ruíz

Recombination is a frequent phenomenon in RNA viruses whose net result is largely influenced by selective pressures. RNA silencing in plants acts as a defense mechanism against viruses and can be used to engineer virus resistance. Here, we have investigated the influence of RNA silencing as a selective pressure to favor recombinants of PVX-HCT, a chimeric Potato virus X (PVX) vector carrying the helper-component proteinase (HC-Pro) gene from Plum pox virus (PPV). All the plants from two lines expressing a silenced HC-Pro transgene were completely resistant to PPV. However a significant proportion became infected with PVX-HCT. Analysis of viral RNAs accumulating in silenced plants revealed that PVX-HCT escaped silencing-based resistance by removal of the HC-Pro sequences that represented preferential targets for transgene-promoted silencing. The virus vector also tended to lose the HC-Pro insert when infecting transgenic plants containing a nonsilenced HC-Pro transgene or wild-type (wt) Nicotiana benthamiana plants. Nevertheless, loss of HC-Pro sequences was faster in nonsilenced transgenic plants than in wt plants, suggesting the transgene plays a role in promoting a higher selective pressure in favor of recombinant virus versions. These results indicate that the outcome of recombination processes depends on the strength of selection pressures applied to the virus.


2009 ◽  
Vol 90 (2) ◽  
pp. 519-525 ◽  
Author(s):  
Sandra Martínez-Turiño ◽  
Carmen Hernández

Viral-derived double-stranded RNAs (dsRNAs) activate RNA silencing, generating small interfering RNAs (siRNAs) which are incorporated into an RNA-induced silencing complex (RISC) that promotes homology-dependent degradation of cognate RNAs. To counteract this, plant viruses express RNA silencing suppressors. Here, we show that the coat protein (CP) of Pelargonium flower break virus (PFBV), a member of the genus Carmovirus, is able to efficiently inhibit RNA silencing. Interestingly, PFBV CP blocked both sense RNA- and dsRNA-triggered RNA silencing and did not preclude generation of siRNAs, which is in contrast with the abilities that have been reported for other carmoviral CPs. We have also found that PFBV CP can bind siRNAs and that this ability correlates with silencing suppression activity and enhancement of potato virus X pathogenicity. Collectively, the results indicate that PFBV CP inhibits RNA silencing by sequestering siRNAs and preventing their incorporation into a RISC, thus behaving similarly to unrelated viral suppressors but dissimilarly to orthologous ones.


2014 ◽  
Vol 95 (3) ◽  
pp. 733-739 ◽  
Author(s):  
Jack H. Westwood ◽  
Mathew G. Lewsey ◽  
Alex M. Murphy ◽  
Trisna Tungadi ◽  
Anne Bates ◽  
...  

The cucumber mosaic virus (CMV) 2b viral suppressor of RNA silencing (VSR) inhibits host responses to jasmonic acid (JA), a chemical signal regulating resistance to insects. Previous experiments with a CMV subgroup IA strain and its 2b gene deletion mutant suggested that VSRs might neutralize aphid (Myzus persicae) resistance by inhibiting JA-regulated gene expression. To further investigate this, we examined JA-regulated gene expression and aphid performance in Nicotiana benthamiana infected with Potato virus X, Potato virus Y, Tobacco mosaic virus and a subgroup II CMV strain, as well as in transgenic plants expressing corresponding VSRs (p25, HC-Pro, 126 kDa and 2b). All the viruses or their VSRs inhibited JA-induced gene expression. However, this did not always correlate with enhanced aphid performance. Thus, VSRs are not the sole viral determinants of virus-induced changes in host–aphid interactions and interference with JA-regulated gene expression cannot completely explain enhanced aphid performance on virus-infected plants.


2006 ◽  
Vol 33 (6) ◽  
pp. 593 ◽  
Author(s):  
Annette Niehl ◽  
Christophe Lacomme ◽  
Alexander Erban ◽  
Joachim Kopka ◽  
Ute Krämer ◽  
...  

A better understanding of defence responses elicited during compatible plant–virus interactions is a current goal in plant pathology. We analysed defence responses during infection of Solanum tuberosum L. cv. Desiree with Potato virus X (PVX) at the transcript and metabolite level. A mostly unchanged primary metabolism reflects the compatible nature of this plant–virus interaction. Salicylic acid biosynthesis and expression of several defence genes including PR-1 and glutathione-S-transferase, which are involved in ethylene and reactive oxygen species dependent signalling, were highly up-regulated in upper-uninoculated (systemic) leaves of PVX-infected potato plants compared with mock-inoculated controls. Moreover, the β-phenylethylamine-alkaloids tyramine, octopamine, dopamine and norepinephrine were highly induced upon infection. β-phenylethylamine-alkaloids can contribute to active plant defence responses by forming hydroxycinnamic acid amides (HCAA), which are thought to increase cell wall stability by extracellular peroxidative polymerisation. Expression of tyramine-hydroxycinnamoyl transferase (THT) and apoplastic peroxidase (POD) was highly induced upon PVX infection in systemic leaves, which suggests synthesis and extracellular polymerisation of HCAA. Since cell-wall-bound ion concentrations could contribute to this process, we measured cell-wall-bound and total ion concentrations in PVX-infected and mock-inoculated leaves. The observed metabolic and transcriptional changes might represent a systemic acquired resistance response against subsequent pathogen challenge.


2003 ◽  
Vol 21 (7) ◽  
pp. 699-704 ◽  
Author(s):  
C. Escobar ◽  
L. E. Hernández ◽  
A. Jiménez ◽  
G. Creissen ◽  
M. T. Ruiz ◽  
...  

2014 ◽  
Vol 89 (4) ◽  
pp. 2090-2103 ◽  
Author(s):  
Emmanuel Aguilar ◽  
David Almendral ◽  
Lucía Allende ◽  
Remedios Pacheco ◽  
Bong Nam Chung ◽  
...  

ABSTRACTMost plant viruses counter the RNA silencing-based antiviral defense by expressing viral suppressors of RNA silencing (VSRs). In this sense, VSRs may be regarded as virulence effectors that can be recognized by the host as avirulence (avr) factors to induceR-mediated resistance. We made use ofAgrobacterium-mediated transient coexpression of VSRs in combination withPotato virus X(PVX) to recapitulate in local tissues the systemic necrosis (SN) caused by PVX-potyvirus synergistic infections inNicotiana benthamiana. The hypersensitive response (HR)-like response was associated with an enhanced accumulation of PVX subgenomic RNAs. We further show that expression of P25, the VSR of PVX, in the presence of VSR from different viruses elicited an HR-like response inNicotianaspp. Furthermore, the expression of P25 by aPlum pox virus(PPV) vector was sufficient to induce an increase of PPV pathogenicity that led to necrotic mottling. A frameshift mutation in the P25 open reading frame (ORF) of PVX did not lead to necrosis when coexpressed with VSRs. These findings indicate that P25 is the main PVX determinant involved in eliciting a systemic HR-like response in PVX-associated synergisms. Moreover, we show that silencing ofSGT1andRAR1attenuated cell death in both PVX-potyvirus synergistic infection and the HR-like response elicited by P25. Our study underscores that P25 variants that have impaired ability to suppress RNA silencing cannot act as elicitors when synergized by the presence of other VSRs. These findings highlight the importance of RNA silencing suppression activity in the HR-like response elicited by VSRs in certain hosts.IMPORTANCEThe work presented here describes how the activity of the PVX suppressor P25 elicits an HR-like response inNicotianaspp. when overexpressed with other VSR proteins. This finding suggests that the SN response caused by PVX-associated synergisms is a delayed immune response triggered by P25, once it reaches a threshold level by the action of other VSRs. Moreover, this work supports the contention that the silencing suppressor activity of PVX P25 protein is a prerequisite for HR elicitation. We propose that unidentified avr determinants could be involved in other cases of viral synergisms in which heterologous “helper” viruses encoding strong VSRs exacerbate the accumulation of the avr-encoding virus.


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